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Swimming Mechanics and Behavior of the Shallow-Water Brief Squid Lolliguncula Brevis

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Swimming Mechanics and Behavior of the Shallow-Water Brief Squid Lolliguncula Brevis W&M ScholarWorks VIMS Articles Virginia Institute of Marine Science 2001 Swimming mechanics and behavior of the shallow-water brief squid Lolliguncula brevis Ian K. Bartol Mark R. Patterson Virginia Institute of Marine Science Roger L. Mann Virginia Institute of Marine Science Follow this and additional works at: https://scholarworks.wm.edu/vimsarticles Part of the Marine Biology Commons Recommended Citation Bartol, Ian K.; Patterson, Mark R.; and Mann, Roger L., Swimming mechanics and behavior of the shallow- water brief squid Lolliguncula brevis (2001). Journal of Experimental Biology, 204, 3655-3682. https://scholarworks.wm.edu/vimsarticles/1452 This Article is brought to you for free and open access by the Virginia Institute of Marine Science at W&M ScholarWorks. It has been accepted for inclusion in VIMS Articles by an authorized administrator of W&M ScholarWorks. For more information, please contact [email protected]. The Journal of Experimental Biology 204, 3655–3682 (2001) 3655 Printed in Great Britain © The Company of Biologists Limited 2001 JEB3819 Swimming mechanics and behavior of the shallow-water brief squid Lolliguncula brevis Ian K. Bartol1,*, Mark R. Patterson2 and Roger Mann2 1Department of Organismic Biology, Ecology, and Evolution, 621 Charles E. Young Drive South, University of California, Los Angeles, CA 90095-1606, USA and 2School of Marine Science, Virginia Institute of Marine Science, College of William and Mary, Gloucester Point, VA 23062-1346, USA *e-mail: [email protected] Accepted 6 August 2001 Summary Although squid are among the most versatile swimmers decreased angles of attack and swam tail-first. Fin motion, and rely on a unique locomotor system, little is known which could not be characterized exclusively as drag- or about the swimming mechanics and behavior of most lift-based propulsion, was used over 50–95 % of the squid, especially those that swim at low speeds in inshore sustained speed range and provided as much as 83.8 % of waters. Shallow-water brief squid Lolliguncula brevis, the vertical and 55.1 % of the horizontal thrust. Small ranging in size from 1.8 to 8.9 cm in dorsal mantle length squid (<3.0 cm DML) used different swimming strategies (DML), were placed in flumes and videotaped, and the from those of larger squid, possibly to maximize thrust data were analyzed using motion-analysis equipment. benefits from vortex ring formation. Furthermore, brief Flow visualization and force measurement experiments squid employed various unsteady behaviors, such as were also performed in water tunnels. Mean critical manipulating funnel diameter during jetting, altering arm −1 swimming speeds (Ucrit) ranged from 15.3 to 22.8 cm s , position and swimming in different orientations, to boost and mean transition speeds (Ut; the speed above which swimming performance. These results demonstrate that squid swim exclusively in a tail-first orientation) varied locomotion in slow-swimming squid is complex, involving from 9.0 to 15.3 cm s−1. At low speeds, negatively buoyant intricate spatial and temporal interactions between the brief squid generated lift and/or improved stability by mantle, fins, arms and funnel. positioning the mantle and arms at high angles of attack, directing high-speed jets downwards (angles >50 °) and Key words: squid, negative buoyancy, hydrodynamics, swimming, using fin activity. To reduce drag at high speeds, the squid jet propulsion, Lolliguncula brevis, fin. Introduction Resistive and propulsive forces associated with jet DeMont (Anderson and DeMont, 2000) focus on the propulsion have been investigated in scallops (Trueman, 1975; hydrodynamics and mechanics of squid locomotion. Johnson Vogel, 1985; Dadswell and Weihs, 1990; Millward and Whyte, et al. (Johnson et al., 1972) outline a theoretical approach to 1992; Cheng and DeMont, 1996; Cheng et al., 1996), jellyfish squid swimming, but it has limited applicability since it is (Daniel, 1983; Daniel, 1985; DeMont and Gosline, 1988), based on one contraction of the mantle musculature and salps (Madin, 1990) and frogfishes (Fish, 1987). The best- incorporates a number of oversimplifications and assumptions. known jetters are cephalopods, including the chambered O’Dor (O’Dor, 1988) provides a more in-depth and Nautilus, octopuses, cuttlefishes and squid. Much of the informative examination of the forces acting on adult squid hydrodynamic work on cephalopods has been performed on Loligo opalescens (and to a lesser extent Illex illecebrosus) Nautilus and centers around the effects of the shell on using video analysis and recordings of mantle cavity pressure. surrounding flow, locomotion and mode of life (Raup, 1967; Anderson and DeMont (Anderson and DeMont, 2000) provide Chamberlain and Westerman, 1976; Chamberlain, 1976; interesting information on propulsive efficiency and some Chamberlain, 1980; Chamberlain, 1981; Chamberlain, 1990; unsteady hydrodynamics of adult Loligo pealei. Holland, 1987; O’Dor et al., 1990). Although there are a The limited research on squid swimming mechanics is number of papers examining swimming energetics of squid surprising given the versatility of squid as swimmers. Squid (O’Dor, 1982; Webber and O’Dor, 1985; Webber and O’Dor, may hover in one spot, change direction rapidly with apparent 1986; O’Dor and Webber, 1986; O’Dor and Webber, 1991; ease, stop and reverse direction and ascend and descend almost O’Dor et al., 1994; Finke et al., 1996), only Johnson et al. vertically. Squid are capable of such impressive maneuvers (Johnson et al., 1972), O’Dor (O’Dor, 1988) and Anderson and because of interactions between three systems: (i) the jet, 3656 I. K. Bartol, M. R. Patterson and R. Mann which may be directed using a funnel maneuverable within a (50–100 cm s−1) (O’Dor, 1982; O’Dor, 1988; Webber and hemisphere below the body, (ii) the fins, which may undulate O’Dor, 1986) and use their fins primarily for maneuvering and and/or flap independently or synchronously, and (iii) the arms, steering (O’Dor, 1988; Hoar et al., 1994), L. brevis appears to which may be positioned at different angles of attack, moved swim at lower speeds (<30 cm s−1), uses considerable fin vertically and laterally and extended and retracted to maximize activity and swims readily in either an arms-first or a tail-first and minimize surface area. orientation (Bartol et al., 2001b). Moreover, there is metabolic Although O’Dor (O’Dor, 1988) and Anderson and DeMont evidence suggesting that brief squid have high swimming costs (Anderson and DeMont, 2000) provide important information at low speeds because of negative buoyancy and have parabolic on moderately large squid species, which swim at moderate to oxygen consumption/speed relationships (Bartol et al., 2001b), high speeds and rely heavily on the jet for propulsion, several which to date have not been detected in Illex illecebrosus, important areas of locomotion in squid remain unexplored. (i) Loligo opalescens and Loligo pealei. Little is known about how swimming mechanics change with To provide insight into how size, swimming orientation, size in squid. With the exception of some general observations unsteady phenomena, fin activity, arm motion and other on Illex illecebrosus hatchlings in aquaria (O’Dor et al., 1985), behaviors affect the swimming mechanics of slow-swimming all hydrodynamic work on squid has focused on adults of squid, brief squid Lolliguncula brevis of various sizes similar size. (ii) Squid are capable of swimming in two swimming in flumes were videotaped, and the footage was orientations: tail-first, in which the posterior closed end of the analyzed using motion-analysis equipment. Subsequent mantle and fins are located at the leading edge and the arms hydrodynamic calculations were based on these data. Flow trail behind, and arms-first, in which the arms are at the leading visualization and force measurement experiments using live edge and the fins and mantle trail behind. However, very little squid and/or models were also performed to investigate is known about arm-first swimming, which is frequently particular aspects of swimming, such as the characteristics of observed in the field and in captivity (Hanlon et al., 1983; the jet wake and the magnitude of lift and drag forces. Because Vecchione and Roper, 1991) and is the primary swimming brief squid appear to possess a unique parabolic relationship mode used for prey capture (Hanlon and Messenger, 1996; between oxygen consumption rate and speed and appear to Kier and van Leeuwen, 1997). (iii) Although the effects of swim over a more restricted speed range than other squid unsteady flow play integral roles in force and lift generation in examined to date, particular emphasis was placed on the effects other aquatic organisms (Daniel, 1983; Daniel, 1984; Daniel, of speed on swimming mechanics. 1988; Dickinson, 1996; Westneat, 1996; Müller et al., 1997; Drucker and Lauder, 1999; Dickinson et al., 2000), unsteady flow effects on squid, which swim in a pulsatile fashion, have Materials and methods received little attention, with the notable exception of a recent Experimental animals study by Anderson and DeMont (Anderson and DeMont, From May to November 1996–1998, brief squid 2000). (iv) Little is known about the swimming mechanics of Lolliguncula brevis (Blainville) were captured by trawl within slow-moving squid, which maneuver in complex, inshore embayments along the seaside of Virginia’s Eastern Shore and environments and appear to use considerable fin motion. (v) within the Chesapeake Bay near Kiptopeke, Virginia. Squid
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